Distinct patterns of functional and effective connectivity between perirhinal cortex and other cortical regions in recognition memory and perceptual discrimination.

Traditionally, the medial temporal lobe (MTL) is thought to be dedicated to declarative memory. Recent evidence challenges this view, suggesting that perirhinal cortex (PrC), which interfaces the MTL with the ventral visual pathway, supports highly integrated object representations in recognition memory and perceptual discrimination. Even with comparable representational demands, perceptual and memory tasks differ in numerous task demands and the subjective experience they evoke. Here, we tested whether such differences are reflected in distinct patterns of connectivity between PrC and other cortical regions, including differential involvement of prefrontal control processes. We examined functional magnetic resonance imaging data for closely matched perceptual and recognition memory tasks for faces that engaged right PrC equivalently. Multivariate seed analyses revealed distinct patterns of interactions: Right ventrolateral prefrontal and posterior cingulate cortices exhibited stronger functional connectivity with PrC in recognition memory; fusiform regions were part of the pattern that displayed stronger functional connectivity with PrC in perceptual discrimination. Structural equation modeling revealed distinct patterns of effective connectivity that allowed us to constrain interpretation of these findings. Overall, they demonstrate that, even when MTL structures show similar involvement in recognition memory and perceptual discrimination, differential neural mechanisms are reflected in the interplay between the MTL and other cortical regions.

[1]  Alan C. Evans,et al.  Volumetry of temporopolar, perirhinal, entorhinal and parahippocampal cortex from high-resolution MR images: considering the variability of the collateral sulcus. , 2002, Cerebral cortex.

[2]  David Gaffan,et al.  Perirhinal cortical contributions to object perception , 2006, Trends in Cognitive Sciences.

[3]  Myra A. Fernandes,et al.  Neural correlates of recollection and familiarity: A review of neuroimaging and patient data , 2007, Neuropsychologia.

[4]  Rainer Goebel,et al.  Common neural substrates for visual working memory and attention , 2007, NeuroImage.

[5]  A. B. Protzner,et al.  Hippocampal–neocortical networks differ during encoding and retrieval of relational memory: Functional and effective connectivity analyses , 2010, Neuropsychologia.

[6]  Malcolm W. Brown,et al.  Recognition memory: What are the roles of the perirhinal cortex and hippocampus? , 2001, Nature Reviews Neuroscience.

[7]  A. McIntosh,et al.  Functional Connectivity of the Medial Temporal Lobe Relates to Learning and Awareness , 2003, The Journal of Neuroscience.

[8]  Norihiro Sadato,et al.  Neural substrates participating in acquisition of facial familiarity: an fMRI study , 2003, NeuroImage.

[9]  M. D’Esposito,et al.  Activity in fusiform face area modulated as a function of working memory load. , 2001, Brain research. Cognitive brain research.

[10]  D. Gaffan,et al.  Impairment of visual object-discrimination learning after perirhinal cortex ablation. , 1997, Behavioral neuroscience.

[11]  Florin Dolcos,et al.  Attention-related activity during episodic memory retrieval: a cross-function fMRI study , 2003, Neuropsychologia.

[12]  Michael D. Rugg,et al.  The Role of the Prefrontal Cortex in Recognition Memory and Memory for Source: An fMRI Study , 1999, NeuroImage.

[13]  Rosemary A. Cowell,et al.  Why Does Brain Damage Impair Memory? A Connectionist Model of Object Recognition Memory in Perirhinal Cortex , 2006, The Journal of Neuroscience.

[14]  Andy C. H. Lee,et al.  Behavioral / Systems / Cognitive Functional Specialization in the Human Medial Temporal Lobe , 2005 .

[15]  Peter Fransson,et al.  Sustained and Transient Neural Modulations in Prefrontal Cortex Related to Declarative Long-Term Memory, Working Memory, and Attention , 2007, Cortex.

[16]  T. Bussey,et al.  Perceptual–mnemonic functions of the perirhinal cortex , 1999, Trends in Cognitive Sciences.

[17]  Michael Petrides,et al.  The mid‐ventrolateral prefrontal cortex: insights into its role in memory retrieval , 2003, The European journal of neuroscience.

[18]  Ellen M. Migo,et al.  Please Scroll down for Article the Quarterly Journal of Experimental Psychology the Contribution of Familiarity to Recognition Memory Is a Function of Test Format When Using Similar Foils , 2022 .

[19]  John Duncan,et al.  Selective Tuning of the Blood Oxygenation Level-Dependent Response during Simple Target Detection Dissociates Human Frontoparietal Subregions , 2007, The Journal of Neuroscience.

[20]  A. Wagner,et al.  Domain-general and domain-sensitive prefrontal mechanisms for recollecting events and detecting novelty. , 2005, Cerebral cortex.

[21]  Michael D. Rugg,et al.  Right dorsolateral prefrontal cortex is engaged during post-retrieval processing of both episodic and semantic information , 2009, Neuropsychologia.

[22]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[23]  Andy C. H. Lee,et al.  Going beyond LTM in the MTL: A synthesis of neuropsychological and neuroimaging findings on the role of the medial temporal lobe in memory and perception , 2010, Neuropsychologia.

[24]  M Petrides,et al.  Architecture and connections of retrosplenial area 30 in the rhesus monkey (macaca mulatta). , 1999, The European journal of neuroscience.

[25]  L. Nyberg,et al.  Common fronto-parietal activity in attention, memory, and consciousness: Shared demands on integration? , 2005, Consciousness and Cognition.

[26]  Karl J. Friston,et al.  PHRENOLOGY : What Can Neuroimaging Tell Us About Distributed Circuitry ? , 2005 .

[27]  Rosemary A. Cowell,et al.  Functional Dissociations within the Ventral Object Processing Pathway: Cognitive Modules or a Hierarchical Continuum? , 2010, Journal of Cognitive Neuroscience.

[28]  E. Rolls,et al.  Selective Perceptual Impairments After Perirhinal Cortex Ablation , 2001, The Journal of Neuroscience.

[29]  Nikolai Axmacher,et al.  Interactions between Medial Temporal Lobe, Prefrontal Cortex, and Inferior Temporal Regions during Visual Working Memory: A Combined Intracranial EEG and Functional Magnetic Resonance Imaging Study , 2008, The Journal of Neuroscience.

[30]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[31]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[32]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[33]  Craig J. Brozinsky,et al.  Functional connectivity with the hippocampus during successful memory formation , 2005, Hippocampus.

[34]  Andy C. H. Lee,et al.  Differentiating the Roles of the Hippocampus and Perirhinal Cortex in Processes beyond Long-Term Declarative Memory: A Double Dissociation in Dementia , 2006, The Journal of Neuroscience.

[35]  W. Suzuki Untangling memory from perception in the medial temporal lobe , 2010, Trends in Cognitive Sciences.

[36]  C. Stark Faculty of 1000 evaluation for How hippocampus and cortex contribute to recognition memory: revisiting the complementary learning systems model. , 2010 .

[37]  Yael Shrager,et al.  Intact Visual Perception in Memory-Impaired Patients with Medial Temporal Lobe Lesions , 2006, The Journal of Neuroscience.

[38]  Matthew Brett,et al.  Dissociable contributions of the mid-ventrolateral frontal cortex and the medial temporal lobe system to human memory , 2006, NeuroImage.

[39]  C. Price,et al.  Perirhinal Contributions to Human Visual Perception , 2007, Current Biology.

[40]  M. D’Esposito,et al.  Dissecting Contributions of Prefrontal Cortex and Fusiform Face Area to Face Working Memory , 2003, Journal of Cognitive Neuroscience.

[41]  Sanghoon Han,et al.  Isolating rule- versus evidence-based prefrontal activity during episodic and lexical discrimination: a functional magnetic resonance imaging investigation of detection theory distinctions. , 2005, Cerebral cortex.

[42]  Pierre Maquet,et al.  Brain activity underlying encoding and retrieval of source memory. , 2002, Cerebral cortex.

[43]  T. Shallice,et al.  Recollection and Familiarity in Recognition Memory: An Event-Related Functional Magnetic Resonance Imaging Study , 1999, The Journal of Neuroscience.

[44]  Benjamin J. Shannon,et al.  Parietal lobe contributions to episodic memory retrieval , 2005, Trends in Cognitive Sciences.

[45]  Edward B. O'Neil,et al.  Perirhinal Cortex Contributes to Accuracy in Recognition Memory and Perceptual Discriminations , 2009, The Journal of Neuroscience.

[46]  M. Baxter Involvement of Medial Temporal Lobe Structures in Memory and Perception , 2009, Neuron.

[47]  Scott A. Huettel,et al.  Rule-dependent Prefrontal Cortex Activity across Episodic and Perceptual Decisions: An fMRI Investigation of the Criterial Classification Account , 2009, Journal of Cognitive Neuroscience.

[48]  G. Luppino,et al.  Cortical connections of the macaque caudal ventrolateral prefrontal areas 45A and 45B. , 2010, Cerebral cortex.

[49]  L. Squire,et al.  Recognition memory and the hippocampus: A test of the hippocampal contribution to recollection and familiarity. , 2010, Learning & memory.

[50]  J. V. Haxby,et al.  Spatial Pattern Analysis of Functional Brain Images Using Partial Least Squares , 1996, NeuroImage.

[51]  Joaquín M. Fuster,et al.  Cortex and Memory: Emergence of a New Paradigm , 2009, Journal of Cognitive Neuroscience.

[52]  Leslie G. Ungerleider,et al.  The neural systems that mediate human perceptual decision making , 2008, Nature Reviews Neuroscience.

[53]  E. Murray,et al.  Preserved Recognition Memory for Small Sets, and Impaired Stimulus Identification for Large Sets, Following Rhinal Cortex Ablations in Monkeys , 1994, The European journal of neuroscience.

[54]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[55]  R. O’Reilly,et al.  Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. , 2003, Psychological review.

[56]  Andy C. H. Lee,et al.  Activating the medial temporal lobe during oddity judgment for faces and scenes. , 2008, Cerebral cortex.

[57]  A. McIntosh,et al.  Mapping cognition to the brain through neural interactions. , 1999, Memory.

[58]  Jia Liu,et al.  Perception of Face Parts and Face Configurations: An fMRI Study , 2010, Journal of Cognitive Neuroscience.

[59]  A R McIntosh,et al.  Functional interactions between the medial temporal lobes and posterior neocortex related to episodic memory retrieval. , 1998, Cerebral cortex.

[60]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[61]  F. Gonzalez-Lima,et al.  Structural equation modeling and its application to network analysis in functional brain imaging , 1994 .

[62]  A. R. McIntosh,et al.  Spatiotemporal analysis of event-related fMRI data using partial least squares , 2004, NeuroImage.

[63]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Projections to the neocortex , 2002, The Journal of comparative neurology.

[64]  Marcia K. Johnson,et al.  Source monitoring 15 years later: what have we learned from fMRI about the neural mechanisms of source memory? , 2009, Psychological bulletin.

[65]  Wendy A. Suzuki,et al.  Perception and the Medial Temporal Lobe: Evaluating the Current Evidence , 2009, Neuron.

[66]  Margot J. Taylor,et al.  Spatio temporal dynamics of face recognition. , 2008, Cerebral cortex.

[67]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[68]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[69]  Andy C. H. Lee,et al.  Medial temporal lobe activity during complex discrimination of faces, objects, and scenes: Effects of viewpoint , 2009, Hippocampus.

[70]  M. Moscovitch Memory and Working-with-Memory: A Component Process Model Based on Modules and Central Systems , 1992, Journal of Cognitive Neuroscience.

[71]  Stefan Köhler,et al.  The missing whole in perceptual models of perirhinal cortex , 2006, Trends in Cognitive Sciences.

[72]  Anthony R. McIntosh,et al.  Memory encoding and hippocampally-based novelty/familiarity discrimination networks , 2003, Neuropsychologia.

[73]  Anthony D Wagner,et al.  Executive Control during Episodic Retrieval Multiple Prefrontal Processes Subserve Source Memory , 2002, Neuron.

[74]  M. Petrides Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[75]  Andrea B Protzner,et al.  Testing effective connectivity changes with structural equation modeling: What does a bad model tell us? , 2006, Human brain mapping.

[76]  J. Haxby,et al.  Neural systems for recognition of familiar faces , 2007, Neuropsychologia.

[77]  M. Petrides,et al.  Efferent association pathways originating in the caudal prefrontal cortex in the macaque monkey , 2006, The Journal of comparative neurology.

[78]  A. McIntosh,et al.  Structural modeling of functional neural pathways mapped with 2-deoxyglucose: effects of acoustic startle habituation on the auditory system , 1991, Brain Research.

[79]  K. Norman How hippocampus and cortex contribute to recognition memory: Revisiting the complementary learning systems model , 2010, Hippocampus.

[80]  Alumit Ishai,et al.  Let’s face it: It’s a cortical network , 2008, NeuroImage.

[81]  L. Saksida,et al.  Impairments in visual discrimination after perirhinal cortex lesions: testing ‘declarative’ vs. ‘perceptual‐mnemonic’ views of perirhinal cortex function , 2003, The European journal of neuroscience.

[82]  E. Maguire,et al.  What does the retrosplenial cortex do? , 2009, Nature Reviews Neuroscience.

[83]  Nicole M. Dudukovic,et al.  Goal-dependent modulation of declarative memory: Neural correlates of temporal recency decisions and novelty detection , 2007, Neuropsychologia.

[84]  R. O’Reilly,et al.  Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans? , 2002, Hippocampus.

[85]  L. Saksida,et al.  Visual perception and memory: a new view of medial temporal lobe function in primates and rodents. , 2007, Annual review of neuroscience.

[86]  Russell A. Epstein,et al.  Perceptual deficits in amnesia: challenging the medial temporal lobe ‘mnemonic’ view , 2005, Neuropsychologia.

[87]  L. Saksida,et al.  Perirhinal cortex resolves feature ambiguity in complex visual discriminations , 2002, The European journal of neuroscience.

[88]  Galia Avidan,et al.  Functional MRI Reveals Compromised Neural Integrity of the Face Processing Network in Congenital Prosopagnosia , 2009, Current Biology.

[89]  H. Spiers,et al.  Prefrontal and medial temporal lobe interactions in long-term memory , 2003, Nature Reviews Neuroscience.

[90]  Kimberly S. Chiew,et al.  A Neural Mechanism Underlying Memory Failure in Older Adults , 2008, The Journal of Neuroscience.

[91]  A. McIntosh,et al.  Modulation of Ventral Prefrontal Cortex Functional Connections Reflects the Interplay of Cognitive Processes and Stimulus Characteristics , 2008, Cerebral cortex.

[92]  R. Cabeza,et al.  Triple dissociation in the medial temporal lobes: recollection, familiarity, and novelty. , 2006, Journal of neurophysiology.